Causes, temporal trends, and the effects of urbanization on admissions of wild raptors to rehabilitation centers in England and Wales

Abstract Data from wildlife rehabilitation centers (WRCs) can provide on‐the‐ground records of causes of raptor morbidity and mortality, allowing threat patterns to be explored throughout time and space. We provide an overview of native raptor admissions to four WRCs in England and Wales, quantifying the main causes of morbidity and mortality, trends over time, and associations between threats and urbanization between 2001 and 2019. Throughout the study period, 14 raptor species were admitted totalling 3305 admission records. The Common Buzzard (Buteo buteo; 31%) and Tawny Owl (Strix aluco; 29%) were most numerous. Relative to the proportion of breeding individuals in Britain and Ireland, Peregrine Falcons (Falco peregrinus), Little Owls (Athene noctua), and Western Barn Owls (Tyto alba) were over‐represented in the admissions data by 103%, 73%, and 69%, respectively. Contrastingly Northern Long‐eared Owls (Asio otus), Western Marsh Harriers (Circus aeruginosus), and Merlin (Falco columbarius) were under‐represented by 187%, 163%, and 126%, respectively. Across all species, vehicle collisions were the most frequent anthropogenic admission cause (22%), and orphaned young birds (10%) were most frequent natural cause. Mortality rate was highest for infection/parasite admissions (90%), whereas orphaned birds experienced lowest mortality rates (16%). For one WRC, there was a decline in admissions over the study period. Red Kite (Milvus milvus) admissions increased over time, whereas Common Buzzard and Common Kestrel admissions declined. There were significant declines in the relative proportion of persecution and metabolic admissions and an increase in orphaned birds. Urban areas were positively associated with persecution, building collisions, and unknown trauma admissions, whereas vehicle collisions were associated with more rural areas. Many threats persist for raptors in England and Wales, however, have not changed substantially over the past two decades. Threats associated with urban areas, such as building collisions, may increase over time in line with human population growth and subsequent urban expansion.


| INTRODUC TI ON
Diurnal and nocturnal raptors are frequently used as ecological indicators due to their high positions within trophic networks (Buechley et al., 2019). Raptor species face a number of threats from anthropogenic activities such as direct and indirect poisoning (Garvin et al., 2020;Hughes et al., 2013), electrocution on powerlines (Lehman et al., 2007), road collisions (Gagné et al., 2015), and human persecution (Murgatroyd et al., 2019;Panter et al., 2021;Smart et al., 2010). For effective conservation programs, the key detrimental impacts of anthropogenic activities need to be identified and evidenced-based conservation measures implemented to alleviate these threats (Hernandez et al., 2018;Holmes et al., 1993;Richardson & Miller, 1997).
Raptor data from wildlife rehabilitation centers provide on-theground records of causes of morbidity and mortality and have been used to evaluate the health status of wild populations (Morishita et al., 1998;Wendell et al., 2002) and to explore trends in anthropogenic threats over time Thompson et al., 2013).
While several previous studies have explored morbidity and mortality of raptors based on admission data to rehabilitation centers, most of these were based on data from a single center, limiting their ability to explore patterns in admission causes over larger spatial scales. To our knowledge, no studies have attempted to explore whether causes of morbidity or mortality differ depending on environmental features and very few have been conducted in the United Kingdom. For example, Kelly and Bland (2006) analyzed admissions, diagnoses, and outcomes of raptors admitted to a center in England, focusing on a single species-the Eurasian Sparrowhawk (Accipiter nisus).
In this study, we compile and analyze raptor admission data from four wildlife rehabilitation centers in western/south-western England and Wales. Firstly, we provide an overview of raptor admissions over a 19-year period (2001-2019), quantifying the most frequently admitted species and the main causes. We then explore whether a number of commonly admitted species and the types (anthropogenic vs natural) or causes of admission have changed over time for one rehabilitation center, for which we had the longest run of data. Over the study period, urban cover in England and Wales has increased (Office for National Statistics, 2021). Therefore, we predict an increase in anthropogenic admissions as a result of increasing human population growth and urban expansion over time (Seto et al., 2012). Certain threats may also have changed over time; for example, over the study period, the number of vehicles in England and Wales has increased (Department of Transport, 2020), and subsequent raptor-vehicle collisions may have also increased over time. Finally, we expect that causes of admission will vary depending on the level of urbanization. For example, we might expect that urbanization increases the probability of admissions due to building or vehicle collisions in line with previous findings (Garcês et al., 2020;Loss et al., 2014). Therefore, we explore whether the level of urbanization (where the individual birds were found) is associated with higher probabilities of certain admission causes.

| Study area
We collated admission records of native raptors admitted to wildlife rehabilitation centers (WRC) located within a study area totalling c. 46,000 km 2 in south-western Britain (Figure 1). The landscape within our study area is not only dominated by agriculture but also includes the major cities of Greater Manchester, Birmingham, Bristol, and Cardiff, which have populations of c. 2.8 million, 2.6 million, 690,000, and 495,000 people, respectively (United Nations,

2014). Our study area also includes the Brecon Beacons National
Park, seven "Areas of Outstanding Natural Beauty" (AONB), and numerous "Sites of Special Scientific Interest" (SSSI) including the West Pennine Moors, Wyre Forest, and Quantock Hills.

| Data collection
Wildlife rehabilitation centers were invited to participate in the study via email correspondence. Four WRC supplied data on raptor admis- birds of prey, conservation, morbidity, mortality, threats, wildlife rescue centers

T A X O N O M Y C L A S S I F I C A T I O N
Conservation ecology; Landscape planning; Urban ecology individual admitted: (1) species, (2) sex (male/female), (3) age (juvenile/ adult; <1 calendar year/>1cy), (4) admission date, (5) cause of admission, (6) location of incident (at the finest spatial scale available), and (7) outcome (deceased/released/kept in captivity). These data spanned a 19-year period from 21st January 2001 to 26th December 2019.

| Classifying causes of morbidity and mortality
To increase comparability with other studies, the classification of admission causes followed categories previously defined by existing studies (see . Upon admission, birds were examined by trained wildlife carers and the admission notes associated with each record were used to assign each admission to the following "types" ("ANTHROPOGENIC," "NATURAL," and "UNKNOWN") and more detailed "causes" (see Appendix S1 for an overview of all admission types, causes, codes, and pooled miscellaneous causes). When causes could not be ascertained, admission type was categorized as "UNKNOWN," which included the causes: "undetermined" (reason unknown and no injury to bird) and "unknown trauma" (reason unknown but the bird was physically injured). F I G U R E 1 Spatial distribution for 14 species of diurnal and nocturnal raptors admitted to four wildlife rehabilitation centers (WRC) between 2001 and 2019 in England and Wales. Geo-referenced admissions with 2-km buffers (N = 1915) shown in relation to urban land cover. Histogram shows the frequency of urban land cover scores within each 2-km buffer and the mean (31%) denoted by the blue dashed line. Map Coordinate Reference System: EPSG 27700 British National Grid

| Landscape and demographic variables
To explore urbanization effects on types and causes of raptor admissions, we used only the geo-referenced admissions (N = 1915). For these, we extracted land cover data and calculated the proportion of urban habitat within a 2-km buffer. Land cover data were downloaded on 30 th April 2020 from the EDINA Environment Digimap Service (Land Cover Map, 2015; https://digim ap.edina.ac.uk/). Land cover data were derived from the "LCM2015" data set in raster format at 25 m resolution, which closely aligned with the timescale of the majority of the admissions. All spatial data extraction was performed in QGIS 3.12.3 with the GRASS 7.4.1 extension (QGIS Development Team, 2019). We reclassified the land cover data using the r.reclass function and a new binary raster layer was created (1 = "urban" + "suburban" and 0 = all other land cover types). Summary statistics were then computed using the base function Zonal Statistics to calculate the percentage of urban cover within each 2-km buffer.

| Statistical analysis
All statistical analyses were performed in R version 3.6.3 (R Core Team, 2020). Data were analyzed using generalized linear models (GLMs) with either binomial (for binary models) or Poisson (for count data) distributions and the respective conical link functions (see Appendix S2 for a list of models). For binomial data, we fitted a twovector response variable using the cbind function. For Poisson GLMs where overdispersion was detected, we fitted the models with a quasi-Poisson distribution.
We explored mortality (binary: 1 = bird died or was euthanised termed "deceased" and 0 = bird released or kept captive termed "not deceased") as a response variable, with explanatory variables of either admission type or cause. We explored trends over time using only data from Gower Bird Hospital, as it was the only WRC with the longest run of data. Using these data, we fitted year as the explanatory variable and fitted a series of separate GLMs with the following response variables: (1) total count of admission each year, irrespec- The effects of urbanization on types and causes of admissions were explored using a series of generalized linear mixed models (GLMMs) in the package "lme4" . For each admission, a binary metric was created (1 = matching admission type and 0 = no match) for each admission type (i.e., anthropogenic, natural, or unknown), or admission cause (where there were ≥30 admissions, i.e., vehicle collisions, trauma, undetermined, orphaned, building collisions, metabolic, infections/parasites and persecution).
These models were then run with "binary admission type/cause" fitted as the response term and "% urban land cover" fitted as the explanatory term. We used binomial error distributions and "logit" link functions with "centreID" included as a random term to control for the lack of independence between admissions from the same center (Appendix S2).
We examined whether certain species were over-and underrepresented within our admissions data by calculating the percentage difference between the relative proportion of breeding individuals in Britain and Ireland, and the proportion of admitted individuals, per species, to each WRC. Breeding population data were derived from the British Trust for Ornithology's BirdFacts database (Robinson, 2005; https://www.bto.org/under stand ing-birds/ birdf acts).

| Admission types and causes
Unknown admission types were the most numerous comprising nearly half of all admissions (n = 1510; 46%), followed by anthropogenic (N = 1215; 37%) then natural admission types (N = 580; 17%; Table 2). Classifying admissions by the more detailed "causes" revealed 855 (26%) of all admissions were associated with "unknown trauma" ( Table 2). The most frequent anthropogenic admission cause was "vehicle collisions" (N = 732; 22% of all admissions; 60% of anthropogenic admissions). For natural admissions, orphaned young birds were the most frequent cause (N = 315; 10% of all admissions, 54% of natural admissions; Table 2).  (Table 2). For the two most admitted diurnal species, the Common Buzzard and Eurasian Sparrowhawk, unknown trauma was the most common admission cause ( Figure 2). Tawny Owls were vehicle collisions and orphaned young birds, comprising 40% and 49% of admissions, respectively (Table 2; Figure 2).

Main admission causes for
Juvenile birds were approximately four times more likely to be admitted due to natural admissions than adults (430 vs. 112 admissions, respectively), and one and half times more likely to be admitted due to metabolic causes, e.g., emaciation or starvation,

| Outcome of admissions
Of all admissions, 60% resulted in the death or euthanasia of the bird, 39% resulted in the release of the bird, and just 1% of birds were kept in captivity post-admission (Table 3). Those admitted for anthropogenic reasons had a significantly higher mortality rate (57%) than those admitted for natural reasons (40%) (z 1,1754 = 6.483, p < .0001) (Figure 3a; Table 3; Appendix S3). Mortality probabilities differed among the most common admission causes (Figure 3b).
Raptors admitted due to infection/parasites had a substantially higher mortality rate (90%) compared with other known admission causes, whereas orphaned birds had a significantly lower mortality rate (16%) than other known admission causes ( Figure 3b; Table 3; Appendix S3).
a Proportions calculated using total diurnal and nocturnal values.
increase in orphaned young birds, admitted to Gower Bird Hospital throughout the study period (Table 4).
We found no significant association between the proportion of urbanization for each geo-referenced admission and the probability that the admission was caused by anthropogenic (z 1,1914 = 0.940, p = .347), natural (z 1,1914 = −1.085, p = .278) or unknown factors (z 1,1914 = −0.118, p = .906). We did, however, find a significant positive association between urbanization and the probability of admission cause being building collisions, persecution, or unknown trauma (Table 5). In the least urbanized areas, the probability of admission being attributed to a building collision was only c. 7% but increased to c. 18% in the most urbanized areas. Likewise, persecution increased from c. 2.5% in the least urbanized areas to around 8% in the most urbanized areas. In contrast, vehicle collision admissions were negatively associated with urbanization, with a considerably higher probability of admissions being attributed to vehicle collisions in less urbanized areas-this was also the case for undetermined admission causes (Table 5). Urbanization was not associated with the probability of admission being attributed to any natural admission causes including infection/parasites, metabolic or orphaned young birds (Table 5).

Compared with the relative proportion of breeding individuals in
Britain and Ireland, some species were under-and over-represented Africa, an analysis of eight years of admissions data for 39 raptor species revealed that vehicle and building collisions were the most common cause of admission (Thompson et al., 2013), and another South African study found that 52% of all admissions for 33 raptor species were also due to collision-related injuries (Maphalala et al., 2021). In our study, collision trauma (both building and vehicle collisions) comprised 56% of all identified admissions and a third of all admissions. In contrast, a 10-year study conducted in Gran Canaria, Spain, found that 65% of raptor admissions were non-trauma-related, e.g., orphaned young birds, with trauma amounting to only around 35% of total admissions (Montesdeoca, Calabuig, Corbera, Rocha, et al., 2017).
Predominate causes of admission to WRC may vary by country.
In Jordan, illegal possession and the transport of raptors was the most common admission cause to a single WRC center between 2017 and 2018, with trauma cases being the second most frequent admission cause (Al Zoubi et al., 2020). A recent study from the Czech Republic reported more than a third of all admissions of 12,923 Common Kestrels to 34 rehabilitation centers were due to nestlings/orphans (Lukesova et al., 2021). In this study, orphans accounted for 14% of total kestrel admissions and together with vehicle collisions were the most frequent admission cause for this species.
In our study, nearly 60% of admitted birds either died or were euthanised. Admissions due to anthropogenic causes had a higher mortality rate (57%) than natural causes (40%), and our more refined analysis suggested that infection/parasite admissions were associated with the highest mortality rates (90%), whereas orphaned birds were associated with the lowest mortality rate (16%). Raptors admitted due to being orphaned tend to have higher survival probabilities than those admitted for other reasons, as evidenced by existing studies (Hanson et al., 2021;Lukesova et al., 2021 [see "Nestlings" and "Incubation" in Table 3]).

| Influence of urbanization on identified causes of admission
The level of urbanization was significantly associated with certain admission causes, with building collisions, persecution, and unknown trauma admissions more likely to occur in more urbanized areas, but with vehicle collisions more likely in rural areas. Compared with diurnal species, nocturnal species are more susceptible to blinding by vehicle headlights (Bullock et al., 2011;Thompson et al., 2013).
Collisions between Tawny Owls and vehicles have been shown to be more common on roads surrounded by increased tree density  (Gomes et al., 2009) where connectivity between territories is higher (Gagné et al., 2015;Santos et al., 2013), i.e., more rural areas, and may explain why vehicle collisions were the most frequent identified admission cause for Tawny Owls in our study. Common Buzzards were the most numerous diurnal species hit by vehicles; the species is less able to adapt to urban habitats (Palomino & Carrascal, 2007) and is also a frequent scavenger of roadkill carcasses in rural areas (Schwartz et al., 2018;Young et al., 2014), which may further explain the increase in vehicle collisions in more rural areas. Vehicle collisions were also the most common admission cause for Western Barn Owls totalling 40% of admissions and were also the most likely cause of death for the species in another study conducted in Britain between 1963-1996 (Newton et al., 1997).
Building collisions were more likely to occur in urban areas with the Eurasian Sparrowhawk being the most frequent species admitted for this reason. This species is an urban adapter often breeding in these environments (Thornton et al., 2017) employing a high-speed attack strategy when hunting avian prey (Newton, 1986). Important causes of mortality have been attributed to collision-based trauma particularly with windows (Newton et al., 1999). A study by Kelly and Bland (2006) analyzed 202 admissions of Eurasian Sparrowhawk to a WRC in England, 32% of admissions were due to collisions, i.e., vehicle and building/window collisions, which is an identical percentage to our findings for this species admitted to four WRC, suggesting that collision-based injuries (and/or death) are relatively common for the species in England and Wales (Newton et al., 1999).  (Petty et al., 2003), preferring to use habitats away from human disturbance (Martínez & Zuberogoitia, 2004), which may partially explain the low numbers observed in our admissions data.
Admission cause in most cases was based upon details from the finder of the bird (usually a member of the public) and an initial assessment by a trained wildlife carer. A veterinary professional (veterinary surgeon or registered veterinary nurse) was usually not involved at this stage, so a definitive clinical diagnosis was not made.
The centers involved, however, all have very experienced and welltrained staff, with the ability to make a good initial assessment of the bird. However, identification accuracy between WRC and trained wildlife carers is unlikely to be equal, which should be considered when making inferences from these data. For 77% of admissions, sex was not determined, constraining our ability to compare admission causes between the sexes. However, the majority of admitted birds were able to be assigned to a broad age category allowing for age-related demographic comparisons.
Nevertheless, 60% of admissions were of adult birds, which support results from WRC in the USA (Hernandez et al., 2018) and Greece (Komnenou et al., 2005). The remaining 40% of admissions comprised juvenile birds and similar patterns have been observed elsewhere; for example, 42% of Northern Long-eared Owl admissions (Italy; Mariacher et al., 2016) and 32% of all raptor admissions (Spain;  being juveniles.

Molina
Relative to anthropogenic admissions, natural admissions are likely to be under-represented in our data due to the majority going unreported (Newton, 2002;Real et al., 2001). The reliance of reports from members of the public means that there is a likely bias towards anthropogenic admission causes. Building and vehicle collisions are more likely to be reported by members of the public by chance than persecution, i.e., illegal activities such as poisoning, gunshot, and trap/snare events. Our data may also include a survivability bias with members of the public more likely to report injured birds that are still alive than those that have already died, inhibiting reliable injury and death estimates at local raptor population levels.
Alternative monitoring methods such as satellite telemetry are more reliable sources for capturing illegal wildlife crimes, as demonstrated by Murgatroyd et al. (2019)

| Implications
Admissions data from WRC have the potential to form important baseline data guiding conservation activities. For example, gunshot admissions data from Greece have been used to advise governmental agencies responsible for hunting regulations (Mazaris et al., 2008) and seasonal cumulative indices have been calculated to explore the potential ecological impacts on local raptor populations in Spain (Molina- . Some 39% of raptors were released back into the wild following treatment; however, the release does not equate to successful reintroduction back into breeding populations.
Post-release monitoring of individuals, for example, via identification of individuals using leg bands and coupled with field surveys, is strongly encouraged. This provides additional conservation value to admissions data and also allows for post-release welfare checks to be made on the bird.
Building and vehicle collisions posed the highest identified risk to raptors in our study area. Increased traffic densities and vehicle speeds have been shown to increase bird-vehicle collision mortalities (Erritzoe et al., 2003). Identification of vehicle collision hotspots along road networks is recommended, and predictive modeling has been applied at the landscape and local scale to improve road safety (Malo et al., 2004). Window decals have successfully reduced average monthly bird-window collisions by 84% (Ocampo-Peñuela et al., 2016). Application of collision prevention decals to the exterior surface of windows (Klem & Saenger, 2012), or tinting of windows (Erickson et al., 2005), are viable solutions to prevent bird-building collisions and citizen science can assist with community-level implementations.
Transformation of natural habitats into human-modified environments has been shown to negatively affect raptor communities, resulting in lower abundances, species richness, and diversity (Carrete et al., 2009). Despite this, some raptor species have shown resilience and even proliferation in urban environments (Cooke et al., 2018;Kettel et al., 2019;. For example , Sumasgutner et al. (2020) found that breeding Peregrine Falcon pairs were more likely to breed and bred earlier in more urbanized areas, compared with their more rural conspecifics, but breeding success may be compromised in more urban areas for some species, e.g., Common Kestrels (Kettel et al., 2018).
Many threats persist for raptors in England and Wales, however, have not changed substantially over the past two decades.
Our findings provide baseline data on the causes of morbidity and mortality of raptors throughout our study area. Threats associated with urban areas, such as building collisions, may increase over time in line with human population growth and subsequent urban expansion. There is potential for future studies to build on our results in an applied context, for example, investigating the financial costs of vehicle damage as a result of vehicle-wildlife collisions.

ACK N OWLED G EM ENTS
We would like to thank Marlies Hebdon (Secret World Rescue) for assistance with data collection and D. Zanders for her useful comments on the draft manuscript. We would like to further thank the following photographers for the use of their Creative Commons im-

CO N FLI C T O F I NTE R E S T
The authors declare no conflict of interest.